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Origin and Adaptation to High Altitude of Tibetan Semi-Wild Wheat

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Origin and Adaptation to High Altitude of Tibetan Semi-Wild Wheat ARTICLE https://doi.org/10.1038/s41467-020-18738-5 OPEN Origin and adaptation to high altitude of Tibetan semi-wild wheat Weilong Guo 1,4, Mingming Xin1,4, Zihao Wang 1,4, Yingyin Yao1, Zhaorong Hu 1, Wanjun Song1, ✉ Kuohai Yu1, Yongming Chen 1, Xiaobo Wang1, Panfeng Guan1, Rudi Appels2,3, Huiru Peng 1 , ✉ ✉ Zhongfu Ni 1 & Qixin Sun 1 Tibetan wheat is grown under environmental constraints at high-altitude conditions, but its 1234567890():,; underlying adaptation mechanism remains unknown. Here, we present a draft genome sequence of a Tibetan semi-wild wheat (Triticum aestivum ssp. tibetanum Shao) accession Zang1817 and re-sequence 245 wheat accessions, including world-wide wheat landraces, cultivars as well as Tibetan landraces. We demonstrate that high-altitude environments can trigger extensive reshaping of wheat genomes, and also uncover that Tibetan wheat acces- sions accumulate high-altitude adapted haplotypes of related genes in response to harsh environmental constraints. Moreover, we find that Tibetan semi-wild wheat is a feral form of Tibetan landrace, and identify two associated loci, including a 0.8-Mb deletion region con- taining Brt1/2 homologs and a genomic region with TaQ-5A gene, responsible for rachis brittleness during the de-domestication episode. Our study provides confident evidence to support the hypothesis that Tibetan semi-wild wheat is de-domesticated from local land- races, in response to high-altitude extremes. 1 State Key Laboratory for Agrobiotechnology, Key Laboratory of Crop Heterosis and Utilization (MOE), Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing 100193, China. 2 AgriBio, Centre for AgriBioscience, Department of Economic Development, Jobs, Transport, and Resources, 5 Ring Road, La Trobe University, Bundoora, VIC 3083, Australia. 3 University of Melbourne, FVAS, Grattan Street, Parkville, VIC 3010, Australia. ✉ 4These authors contributed equally: Weilong Guo, Mingming Xin, Zihao Wang. email: [email protected]; [email protected]; [email protected] NATURE COMMUNICATIONS | (2020) 11:5085 | https://doi.org/10.1038/s41467-020-18738-5 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-020-18738-5 nderstanding the evolution and domestication of plants chromosomes with the aid of the Chinese Spring (CS) IWGSCv1 Uhas accelerated crop breeding through being able to target reference genome11. A total of 95.51% scaffolds were ordered to new germplasm for crossing into elite lines and creating a form the 21 high-confidence pseudochromosomes, comprising more secure world food supply1–3. Hexaploid or bread wheat 1067 scaffolds with 14.05 Gb (Fig. 1b), which is similar to that of (Triticum aestivum, AABBDD) is a staple food crop for more the reference CS genome (14.07 Gb)11. The Zang1817 genome than one-third of the world population4 and originated ~10,000 assembly reported here is a sequenced genome of a semi-wild years ago in the Near-Eastern Fertile Crescent through hybridi- form of hexaploid wheat to date. zation between domesticated tetraploid wheat, Triticum turgidum A total of 118,078 high-confidence protein-coding genes were (AABB) and wild goatgrass, Aegilops tauschii (DD)5. As a tem- inferred from the Zang1817 assembly using protein-homology- perate crop, hexaploid wheat is widely distributed around the based prediction methods supported by RNA-sequencing data. world, including the Tibetan Plateau, which has an average alti- Repetitive elements, a major component of complex genomes, tude of 4268 m above sea level6, and is characterized by extensive were widely dispersed throughout the wheat genome11,12.Upto UV-B irradiation, extremely low temperature and strong hypoxia 82.74% of the Zang1817 assembly sequence were annotated as stress. Although such environmental constraints would be repeat sequences, including retrotransposons (63.91%), DNA expected to trigger genomic variation of wheat associated with transposons (18.45%) and other unclassified sequence (1.57%). adaptation to high-altitude (HA), the underlying molecular Copia and Gypsy family retrotransposons accounted for ~44.16% changes are still unknown. Thus, Tibetan wheat provides a sig- and 15.28% of the Zang1817 assembly sequence, respectively nificant resource to understand genomic adaptation to the (Supplementary Table 1). The composition of the different classes environmental extremes at high altitude conditions. In addition, of repetitive DNA in Zang1817 was highly similar to that in the although wild forms of bread wheat are not found, a unique CS genome. We further evaluated the annotation with 1440 Tibetan semi-wild hexaploid wheat (Triticum aestivum ssp. tibe- Benchmarking Universal Single Copy Orthologs (BUSCO)13 tanum Shao) is discovered on the Tibetan Plateau, China7. Huang genes, and found 99.51% genes were recalled in the genome, and his colleagues6 investigated 17 agronomic traits of 77 Tibetan with 94.38~96.81% among the three subgenomes individually, a accessions and 277 Tibetan semi-wild wheat, and found that percentage similar to that of the CS genome (99.72%), thus Tibetan semi-wild wheat phenotypically resembles Tibetan local indicating a near completeness of Zang1817 genome assembly landraces but differs in brittle rachis characteristics (Fig. 1a). (Supplementary Table 2). Thus, they suspected that Tibetan semi-wild wheat was a de- Extensive genomic variations have been reported in maize and domesticated form of Tibetan local landraces as a result of natural rice14,15. We found that genomic variation between Zang1817 selection. Yet, no genetic or genomic evidence is provided to and CS, when the pseudochromosomes were aligned, mainly support this hypothesis. Brittle rachis is generally controlled by occurred in non-coding regions. By comparing the two genomes, genes on the short arm of the group 3 chromosomes, especially we determined the present/absent variation (PAV) for segments chr3D8, as well as alleles of the Q locus on 5A9. However, there is longer than 10 kb (Fig. 1c) and identified 345.73 Mb Zang1817- a lack of understanding of the genomic variations that contribute specific genomic segments, including 1875 Zang1817-specific to the Tibetan wheat wild-like traits at the population scale. genes compared with CS (Supplementary Data 1). GO analysis To address these knowledge gaps, we de novo assemble the revealed that these genes were predominantly enriched in genome sequence of a high-altitude wheat accession (Tibetan “polysaccharide binding” (GO:0030247) and “serine-type endo- semi-wild wheat Zang1817), and resequence 245 wheat acces- peptidase inhibitor activity” (GO:0004867) categories. We also sions, including Tibetan semi-wild wheat accessions, Tibetan identified 389.29 Mb of genomic segments containing 2540 genes landraces and cultivars, representing the largest resequencing of that were absent from the Zang1817 assembly in comparison with world-wide wheat landraces and accessions to date. In combi- CS genome (Supplementary Data 2). These genes were mostly nation with previously published 73 re-sequenced accessions10, involved in photosynthesis related GO terms including “photo- we demonstrate that adaptation to high-altitude environments system II reaction center” (GO:0009539), “chloroplast thylakoid likely trigger extensive reshaping of the wheat genomes. In par- membrane” (GO:0009535), “photosynthesis, light reaction” ticular, we argue that the TaHY5-like-mediated signaling pathway (GO:0019684) and “cytochrome b6f complex” (GO:0009512). might play a role in the adaptation to high-altitude extreme Interestingly, the PAV genes were unevenly distributed across the environments in Tibetan wheat and possibly other plants. Fur- genome and tended to be distributed at the ends of chromosomes thermore, we uncover a feral origin of Tibetan semi-wild wheat, and devoid in centromeric regions (Fig. 1d). A genomic inversion which is probably, in effect, a de-domesticated form of Tibetan at 366~375 Mb region of chromosome 6D in Zang1817 was landraces, suggesting that the Tibetan wheat is a resource for fine revealed based on the genomic comparison, which shared a fine tuning wheat germplasm to certain environments. collinearity between Zang1817 assembly and Aegilops tauschii genome12 (Supplementary Fig. 1), further validating the high- quality of the Zang1817 genome assembly. Results The α-gliadin genes confer wheat the unique viscoelastic De novo assembly of Tibetan semi-wild wheat Zang1817 gen- properties, which facilitate the processing of flour into bread, ome. Genomic variation in HA adapted wheat compared with pasta, noodles, and other food products. An in-depth sequence low-altitude (LA) wheat was determined by generating a de novo comparison of the terminal regions of the chromosome group 6 genome assembly of Tibetan semi-wild wheat Zang1817. First, we indicated that the duplication and expansion of α-gliadin genes in generated >240× coverage sequencing reads from a series of PCR- the three homeologous groups occurred extensively in Zang1817 free Illumina paired-end libraries and mate-paired libraries. The assembly compared with CS genome. For example, the 2.4 Mb contig and scaffold assembly was performed using the region at 25.91–28.31 Mb on chromosome 6 A from the DeNovoMAGIC3 software platform (NRGene, Nes Ziona, Israel), Zang1817 genome contained 34 α-gliadin genes, more than triple and additional Chromium 10X genomic data were utilized to the number from the CS genome (9, region at 24.92–26.84 Mb), support scaffold
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